BODY SIZE AND FLIGHT RANGE IN STINGLESS BEES 563

BODY SIZE AND FLIGHT DISTANCE IN STINGLESS BEES (: MELIPONINI): INFERENCE OF FLIGHT RANGE AND POSSIBLE ECOLOGICAL IMPLICATIONS

ARAÚJO, E. D.,1 COSTA, M.,2 CHAUD-NETTO, J.2 and FOWLER, H. G.3 1Grupo de Pesquisa em Comportamento , ITP, UNIT, CEP 49032-490, Aracaju, SE, Brazil 2Departamento de Biologia, Instituto de Biociências, UNESP, Av. 24-A, 1515, C.P. 199, CEP 130506-900, Rio Claro, SP, Brazil 3Departamento de Ecologia, Instituto de Biociências, UNESP. Av. 24-A, 1515, C.P. 199, CEP 130506-900, Rio Claro, SP, Brazil Correspondence to: Edilson D. Araújo, Laboratório de Zoologia, ITP, UNIT, CEP 49032-490, Aracaju, SE, Brazil, e-mail: [email protected] Received February 4, 2003 – Accepted April 30, 2003 – Distributed August 31, 2004 (With 2 figures)

ABSTRACT

We examined the spatial implications of maximum flight distance for several species of stingless bees. Data suggested that maximum flight distance in Meliponini is a function of body size, especially gen- eralized wing size, which can be estimated through principal component analysis. For six species of stingless bees, flight distances and generalized wing sizes were highly correlated (r = 0.938). This in- dicates that species of Meliponini occupy an effectively larger area as body size increases, which has important implications in the spatial dynamics of local populations restricted to forest fragments. We also used the fitted linear regression model to estimate the maximum flight distance for 12 other species of Meliponini. The results of this research may provide insights for future studies of biological conservation. Key words: flight distance, local populations, morphometry, multivariate analysis.

RESUMO

Tamanho do corpo em Meliponini (Hymenoptera: ): inferência do raio de vôo e possíveis implicações ecológicas Neste trabalho analisamos as implicações espaciais da distância máxima de vôo para algumas espécies de meliponíneos. Os dados sugerem que a distância máxima de vôo em meliponíneos está relacionada ao tamanho do corpo, especialmente ao tamanho generalizado das asas, que pode ser estimado utilizando análises de componentes principais. Uma análise utilizando seis espécies de meliponíneos evidenciou que o tamanho generalizado das asas está fortemente correlacionado à distância de vôo (r = 0,938). Isso sugere que espécies de meliponíneos ocupam área efetivamente maior quanto maior for o tamanho do corpo, trazendo importantes implicações para a dinâmica espacial de populações locais restritas a áreas fragmentadas. Neste trabalho, também utilizamos um modelo de regressão linear a fim de estimar as distâncias máximas de vôo para 12 outras espécies de meliponíneos. Esta pesquisa fornece subsídios para futuros estudos relacionados à conservação da biodiversidade. Palavras-chave: distância de vôo, populações locais, morfometria, análise multivariada.

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INTRODUCTION an orthogonal analysis to transform it into a new non-correlated variable set, whose variances decline Meliponini are eusocial bees which are in each principal component, in such a way that the abundant in subtropical and tropical regions of the first principal component explains the major part world, and comprise one of the most diverse and of the variance present in the original characters important groups. The stingless bees have (Reis et al., 1988). A logarithmic data transformation an important ecological role, especially in the is generally used to correct for nonlinearity produced pollination of a large fraction (40% to 90%) of the by the allometry among differing morphological plants forming Brazilian forests (Kerr et al., 1994). characters (Gould, 1966; Neff & Marcus, 1980). Data of maxima flight distances of stingless Species studied and their identification codes were: bee workers are important for tropical ecosystems (Pb) Plebeia droryana Friese (1900), (Ts) Trigona (Roubik & Aluja, 1983) and may even be used to spinipes Fabricius (1793), (Mc) Melipona com- formulate models of population dynamics of pressipes Fabricius (1804), (Mq) Melipona different species. Studies of flight distances, in quadrifasciata Lepeletier (1836), (Mm) Melipona conjunction with other studies of local populations, marginata Lepeletier (1836), and (Cc) can generate important inferences on migration, capitata Smith (1854), which were colonization, forest fragmentation, and biodiversity chosen because flight distances for these bees can conservation. easily be found in the literature. Flight distances have been studied for only a Morphometric characters were measured using few species and generally utilize indirect the criteria of Cunha (1973, 1991) and are given methods of release and recapture (Roubik, 1989). in Table 1, as well as the respective score for each Apparently, there is no directional interference in of the six species studied. flight activities, and the number of marked honey Flight distance data were taken from publi- bees (Apis mellifera) collected declines linearly in cations which used mark-recapture methods. Roubik relation to distance from the colonies (Paranhos et & Aluja (1983) used a magnetic recapture method al., 1997). There is an apparent positive correlation and through regression analysis concluded that the between body size, especially wing area, and flight maximum flight distance for workers of distances (Casey et al., 1985; Byrne et al., 1988). Cephalotrigona capitata was 1,650 m. In Melipona Schwarz (1948) suggested that, because they marginata, maximum flight distance is 800 m. strengthen wing stability, wing hamuli in greater (Wille, 1983). Kerr (1987) recorded a flight dis- number are associated with larger flight capacity. tance of 2,000 m for Melipona quadrifasciata; 840 Worker bee size reflects an adaptation to m for Trigona spinipes; 2,470 m for Melipona environmental conditions (Ruttner, 1988). A major compressipes; and 540 m for Plebeia droryana. part of the morphological variation in Meliponini Two principal component analyses were per- occurs independently of phylogeny due to the fact that, formed. One analysis used generalized body size, for social bees, worker body size has been generally employing all the morphometric variables; the other considered as an adaptation to foraging activity and used only wing variables. First principal component floral resource exploitation (Roubik & Ackerman, scores, for each of these analyses, together with the 1987; Baumgartner & Roubik, 1989). About 75.5% flight distances for each species, were used to form of body size variation in Meliponini corresponds to two new matrices which were examined with a linear adaptive factors associated with resource exploitation regression analysis (Zar, 1999). A third regression (Pignata & Diniz-Filho, 1996). Here we examine the analysis was performed using log values of the spatial implications of maximum flight distance for number of wing hamuli for each of the six species several species of stingless bees. studied in relation to their respective flight distances. Upon fitting of the linear regression model, MATERIAL AND METHODS a new matrix was created with data from the 11 characters of the wing (characters number 18 to 28 Variation in worker body size of six species of Table 1) of 12 other species of Meliponini. This of Meliponini was studied using principal com- new covariance matrix, following the same pattern ponent analysis (PCA) based on covariance matrices. as in the previous analysis, was converted into 11 The PCA uses the original variable set and performs log-transformed characters and subjected to a PCA.

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TABLE 1 Measured morphological characters and their scores in the six stingless bee species analyzed (P. droryana – Pd, T. spinipes – Ts, M. compressipes – Mc, M. quadrifasciata – Mq, M. marginata – Mm, and C. capitata – Cc).

N Character Pd Ts Mc Mq Mm Cc 1 Length of the antennal flagellus 1.125 1.825 3.100 2.835 0.975 2.425 2 Scape length 0.525 0.925 1.500 1.400 1.025 1.225 3 Mandibular length 0.525 0.925 1.575 1.550 1.025 1.175 4 Inter-malar distance 0.800 1.250 1.625 1.500 1.125 1.400 5 Glossa length 0.950 1.800 2.765 2.475 1.875 2.125 Distance between the central ocellus and the clypeus 6 0.850 1.550 2.500 2.375 1.625 2.200 along the frontal line 7 Inter-ocular distance at the central ocellus 0.625 1.325 2.275 1.800 1.375 1.450 8 Inter-ocular distance along the frontal-clypeus suture 0.400 0.500 1.175 1.225 0.925 0.950 9 Clipeal length 0.200 0.350 0.575 0.475 0.325 0.450 10 Inter-alveolar distance 0.300 0.450 0.700 0.600 0.500 0.525 11 Distance between lateral ocelli 0.225 0.525 0.725 0.750 0.400 0.625 Distance between the lateral ocellus and the 12 0.950 1.800 2.800 2.125 1.625 0.875 compound eye 13 Femur length 1.250 2.800 3.750 3.220 2.150 1.225 14 Tibial length 0.425 0.875 1.425 1.125 0.850 0.500 15 Maximum width of the tibia 0.650 1.125 1.950 1.625 1.175 0.475 16 Basitarsal length 0.275 0.575 1.000 0.825 0.550 0.275 17 Maximum width of the basitarsus 3.600 6.900 9.200 7.800 5.400 7.900 18 Maximum length of the fore wing 1.350 2.475 3.250 2.900 1.925 2.905 19 Maximum width of the fore wing 0.925 1.500 1.800 1.300 1.000 1.900 20 M nerve length 0.100 0.075 0.300 0.225 0.150 0.100 21 Rs nerve length 1.000 1.750 2.870 2.425 1.725 2.200 22 Anal nerve length 0.950 1.800 2.590 2.475 1.650 2.150 23 M + cubital nerve length 0.750 1.350 1.820 1.350 1.000 1.650 24 Cubital nerve length 0.225 0.375 0.550 0.475 0.325 0.450 25 Cubital transverse nerve length 0.100 0.200 0.350 0.300 0.175 0.200 26 Cubital + anal nerve length 2.695 4.600 6.600 6.000 3.950 5.500 27 Maximum length of the hind wing 0.675 1.150 1.775 1.450 1.000 1.225 28 Maximum length of the fore wing 0.125 0.125 0.350 0.250 0.250 0.200 29 Number of hamuli 1.050 1.750 3.150 3.080 2.000 2.400 30 Maximum length between tegula 0.975 1.375 3.150 2.940 1.825 1.775 31 Maximum length of the mesoscutum 0.300 0.575 1.050 0.375 0.625 0.550 32 Maximum length of the scutellum 1.119 1.390 3.867 3.320 2.340 2.907

The character scores of the first principal RESULTS component were subjected to the same linear regression model as before, which was then used Estimated flight distances for the six species of to estimate the maximum flight distance for each Meliponini and the scores of the principal component of these 12 species. Analyses were performed using analysis were used to form two new matrices. Scores SYSTAT, version 5.01 for Windows. from the first principal component for the 32

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morphological characters represented the species- colonies of Apis mellifera show no directional specific generalized body size, which was highly interference in flight activities. This indicates that correlated with data of flight distances (r = 0.897). each colony occupies a central position in relation A linear regression analysis indicated that more than to flight radius, defining an effective area corres- 75% of the variation in the maximum flight distance ponding to the circumference described by the could be attributed to generalized worker body size medium flight radius in their components. (adjusted R2 = 0.755). We then examined the log- Our results also suggest that stingless bees transformed values of the number of hamuli, which occupy a maximum effective space proportional produced a fit with maximum flight distance similiar to body size, especially with wing dimensions, which to that obtained for generalized body size (adjusted might constitute strong constraints on local popu- R2 = 0.757). These results are, however, congruent lations restricted to forest fragments. Habitat frag- with the suggestion of Schwarz (1948) that a greater mentation occurs when a large continuous area is number of wing hamuli is associated with larger flight reduced, creating one or more habitat fragments capacity. However, when we performed a linear (Lovejoy et al., 1986; Wilcove et al., 1986). These regression analysis using only scores of species-specific fragments of the original habitat are frequently generalized wing size, these were highly correlated isolated by degraded and highly modified areas. with maximum flight distance (r = 0.938) (Fig. 1). When a habitat is fragmented, dispersion and Therefore, more than 84% of the maximum flight potential colonization is frequently reduced. Many distance variation can be explained by generalized wing species of birds, mammals, and of the in- size (adjusted R2 = 0.849). This suggests that, as in terior forest will not cross small distances of open the Euglossinae (Casey et al., 1985) and in Homoptera areas (Lovejoy et al., 1986; Bierregaard et al., 1992). (Byrne et al., 1988), Meliponini wing size explains In the Meliponini, genetic drift is an extremely a large fraction of maximum flight capacity. important factor in the isolation of small local Using the fitted linear regression, maximum populations. Araújo (2000) suggested that popu- flight distance = 1,383.333 + 645.185 (generalized lations of Melipona are particularly sensitive to the wing size) + error, we estimated the maximum flight effects of genetic drift due to homozygosity in the distance for 12 additional species of Meliponini from Xo sex determination locus. Carvalho et al. (1995) their generalized wing size. For small bees documented the loss of alleles and the extinction Tetragonisca angustula Latreille (1836), Scaura of local populations due to low population number. latitarsis Friese (1900), Plebeia poecilochroa Moure Kerr & Vencovsky (1982) estimated that a & Camargo (1993), and Nannotrigona testaceicornis Meliponini population should contain a minimum Lepeletier (1836), maximal flight distances ranged of 44 colonies to lower the risks of rapid extinction. from 621 to 951 m (Fig. 2). Maximal flight distances Our results suggest that the risk of extinction for medium-sized species Trigona hypogea Silvestri is greater for smaller stingless bees. Colonies of (1902), Trigona recursa SMITH (1863), Geotrigona Plebeia droryana would be effectively isolated if inusitata Moure & Camargo (1991), Frieseomelitta inter-fragment distances were greater than 600 m. varia Lepeletier (1836), Partamona cupira Smith On the other hand, larger species, such as Melipona (1863) and Scaptotrigona postica Latreille (1807) compressipes and Melipona quadrifasciata, would ranged from 1159 to 1710 m (Fig. 2). Estimated flight be effectively isolated if forest fragments were distances for larger bees Melipona bicolor Lepeletier greater than 2 km apart. However, larger species (1836) and Melipona scutellaris Latreille (1811), were theoretically have a greater capacity to migrate greater than 2 km (Fig. 2). It should be pointed out between forest fragments, but would also depend that each estimated value represents a mean expec- upon larger areas to persist. tation of the maximum flight distance for each In the stingless bees, body size could act as species, with an associated error. a limiting factor in maximum flight capacity. Never- theless, it is possible that many species in fact DISCUSSION occupy an effectivly smaller space, depending on the influence of other variables such as: foraging These data suggest further need for research behavior related to specialization in the search for of the spatial dynamics of local populations of specific floral resources, manners of orientation and Meliponini. Paranhos et al. (1997) observed that trail laying, localization and abundance of food

Braz. J. Biol., 64(3B): 563-568, 2004 BODY SIZE AND FLIGHT RANGE IN STINGLESS BEES 567

resources, and availability of nest sites, among stingless bees generally provide the new nest with others. Swarming activity in Meliponini could also food and materials (Nogueira-Neto, 1997). act as a limiting factor of the spatial distribution Therefore, maximum flight distance, conditioned of nests, since a new colony of meliponins is by body size, must have a direct influence on the strongly dependent on the parental nest from which dispersion capacity of the population.

y = 1,383.333 + 645.185 * x + e 2800

M. compressipes 2400 ) m (

M. quadrifasciata

e 2000 c n a t s

i C. capitata d

1600 t h g i l F 1200

T. spinipes 800 M. marginata P. droriana 400 –2.5 –2 –1.5 –1 –0.5 0 0.5 1 1.5 2

Generalized wing size

Fig. 1 — Linear regression of generalized wing size (from the first principal component) against maximum flight distance for several species of stingless bees. Dotted lines represent confidence intervals (α = 0.05).

y = 1,383.333 + 645.185 * x + e

–2.4

Fig. 2 — Maximum flight distances for 12 species of Meliponini estimated using a linear regression model. Dotted lines show the confidence interval (α = 0.05), based upon the linear regression of six documented species (Fig. 1).

Braz. J. Biol., 64(3B): 563-568, 2004 568 ARAÚJO, E. D. et al.

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